Eur. J. Entomol. 115: 450-454, 2018 | DOI: 10.14411/eje.2018.046

Pseudoparasitism by Spalangia cameroni (Hymenoptera: Pteromalidae) of pupae of Ceratitis capitata (Diptera: Tephritidae): Frequency and implicationsOriginal article

Luis DE PEDRO1,2, Francisco BEITIA2, Josep D. ASÍS1, José TORMOS1
1 Área de Zoología, Facultad de Biología, Universidad de Salamanca, 37007-Salamanca, Spain; e-mails: ldepedro@usal.es, tormos@usal.es, asis@usal.es
2 Instituto Valenciano de Investigaciones Agrarias, Unidad Asociada de Entomología IVIA/CIB-CSIC, Apartado Oficial, 46113-Montcada, Valencia, Spain; e-mail: beitia_fra@gva.es

The effectiveness of natural enemies in controlling pests may be determined by many traits linked to their ability to regulate the density of their prey. In this respect, the phenomenon of pseudoparasitism, in which female parasitoids reject a host after inserting their ovipositor into it, is fairly common among hymenopteran parasitoids. However, in spite of this its effect on hosts is rarely reported in entomological and biological control literature. For this reason, in the present study, the pseudoparasitism by the parasitoid Spalangia cameroni Perkins of the Mediterranean pest Ceratitis capitata (Wiedemann) and its effect on several biological parameters of the host were studied under laboratory conditions. The results indicate that the percentage pseudoparasitism by S. cameroni of medfly in the laboratory is high, even slightly higher than host-feeding, which is commonly used to evaluate the potential of parasitoids as biological control agents. In addition, the adults that emerge from pseudoparasitized medfly pupae have a male-biased sex ratio, low levels of survival and are frequently damaged, which results in small adults and an inability to mate successfully. In conclusion, our results indicate that pseudoparasitism is common and enhances the effectiveness of S. cameroni attacking medfly, which highlights the importance of this phenomenon when selecting parasitoids to be included in a biological control programme.

Keywords: Hymenoptera, Pteromalidae, Spalangia cameroni, Diptera, Tephritidae, Ceratitis capitata, Mediterranean fruit fly, parasitoid, pseudoparasitism, overstinging, biological control

Received: April 20, 2018; Revised: July 20, 2018; Accepted: July 20, 2018; Published online: August 29, 2018  Show citation

ACS AIP APA ASA Harvard Chicago Chicago Notes IEEE ISO690 MLA NLM Turabian Vancouver
DE PEDRO, L., BEITIA, F., ASÍS, J.D., & TORMOS, J. (2018). Pseudoparasitism by Spalangia cameroni (Hymenoptera: Pteromalidae) of pupae of Ceratitis capitata (Diptera: Tephritidae): Frequency and implications. EJE115, Article 450-454. https://doi.org/10.14411/eje.2018.046
Download citation

References

  1. Abram P.K., Brodeur J., Burte V. & Boivin G. 2016: Parasitoid-induced host egg abortion: an underappreciated component of biological control services provided by egg parasitoids. - Biol. Contr. 98: 52-60. Go to original source...
  2. Albajes R. & Santiago-Álvarez C. 1980a: Efectos de la densidad larvaria y de la alimentación en la proporción de sexos de Ceratitis capitata (Diptera, Trypetidae). - An. Inst. Nac. Invest. Agr. (Ser. Agríc.) 13: 175-182.
  3. Albajes R. & Santiago-Álvarez C. 1980b: Influencia de la temperatura en el desarrollo de Ceratitis capitata (Diptera, Trypetidae). - An. Inst. Nac. Invest. Agr. (Ser. Agríc.) 13: 183-190.
  4. Beitia F., Valencia E., Peris B., de Pedro L., Asís J.D. & Tormos J. 2016: Influence of natal host on parasitism by Spalangia cameroni (Hymenoptera: Pteromalidae). - Eur. J. Entomol. 113: 99-103. Go to original source...
  5. Biondi A., Desneux N., Amiens-Desneux E., Siscaro G. & Zappalà L. 2013: Biology and developmental strategies of the palaearctic parasitoid Bracon nigricans on the neotropical moth Tuta absoluta. - J. Econ. Entomol. 106: 1638-1647. Go to original source...
  6. Birkemoe T., Soleng A. & Aak A. 2009: Biological control of Musca domestica and Stomoxys calcitrans by mass releases of the parasitoid Spalangia cameroni on two Norwedian pig farms. - BioControl 54: 425-436. Go to original source...
  7. Bloem K., Bloem S., Chambers D. & Muniz E. 1993: Field evaluation of quality: release-recapture of sterile medflies of different sizes. In Aluja M. & Liedo P. (eds): Fruit Flies: Biology and Management. Springer, New York, pp. 295-296. Go to original source...
  8. Boller E.F., Remund U. & Katsoyannos B. 1977: Quality control in European cherry fruit fly: evaluation of mating activity in laboratory and field-cage tests. - J. Appl. Entomol. 83: 183-201. Go to original source...
  9. Brown J.J. & Kainoh Y. 1992: Host castration by Ascogaster sp. (Hymenoptera: Braconidae). - Ann. Entomol. Soc. Am. 85: 67-71. Go to original source...
  10. Cebolla R., Vanaclocha P., Urbaneja A. & Tena A. 2018: Overstinging by hymenopteran parasitoids causes mutilation and surplus killing of hosts. - J. Pest Sci. 91: 327-339. Go to original source...
  11. Churchill-Stanland C., Stanland R., Wong T.T.I., Tanaka N., McInnis D.O. & Dowell R.V. 1986: Size as a factor in the mating propensity of Mediterranean fruit flies, Ceratitis capitata (Diptera: Tephritidae), in the laboratory. - J. Econ. Entomol. 79: 614-619. Go to original source...
  12. de Pedro L., Beitia F., Ferrara F., Asís J.D., Sabater-Muñoz B. & Tormos J. 2017: Effect of host density and location on the percentage parasitism, fertility and induced mortality of Aganaspis daci (Hymenoptera: Figitidae), a parasitoid of Ceratitis capitata (Diptera: Tephritidae). - Crop Prot. 92: 160-167. Go to original source...
  13. EPPO 2012: PQR - EPPO Database on Quarantine Pests. URL: http://www.eppo.int (last accessed 16 Feb. 2018).
  14. Falcó J.V., Garzón-Luque E., Pérez-Hinarejos M., Tarazona I., Malagón J. & Beitia F. 2006: Two native pupal parasitoids of Ceratitis capitata (Diptera, Tephritidae) found in Spain. - IOBC/WPRS Bull. 29: 71-74.
  15. Fletcher B.S. 1989: Life history strategies of tephritid fruit flies. In Robinson S. & Hooper G. (eds): Fruit Flies: Their Biology, Natural Enemies and Control. Elsevier, Amsterdam, pp. 195-209.
  16. Gerling D. & Legner E.F. 1968: Developmental history and reproduction of Spalangia cameroni, parasite of synanthropic flies. - Ann. Entomol. Soc. Am. 61: 1436-1443. Go to original source...
  17. Hegazi E.M. & Khafagi W.E. 2000: Possible bases of pseudoparasitism in Spodoptera littoralis larvae stung by Microplitis rufiventris. - J. Insect Physiol. 46: 1267-1274. Go to original source...
  18. Iga M. 1981: Mating preference of Dacus dorsalis (Hendel) (Diptera: Tephritidae) with reference to individual variations in size. - J. Appl. Entomol. 25: 292-294. Go to original source...
  19. Johnson D., Akre B.G. & Crowley P.H. 1975: Modeling arthropod predation: wasteful killing by damselfly naiads. - Ecology 56: 1081-1093. Go to original source...
  20. Jones D. 1985: Parasite regulation of host insect metamorphosis: a new form of regulation in pseudoparasitized larvae of Trichoplusia ni. - J. Comp. Physiol. 155: 583-590. Go to original source...
  21. Jones D., Jones G., Rudnicka M., Click A., Reck-Malleczewen V. & Iwaya M. 1986: Pseudoparasitism of host Trichoplusia ni by Chelonus spp. as a new model system for parasite regulation of host physiology. - J. Insect Physiol. 32: 315-328. Go to original source...
  22. King B.H. 1988: Sex-ratio manipulation in response to host size by the parasitoid wasp Spalangia cameroni: a laboratory study. - Evolution 42: 1190-1198. Go to original source...
  23. King B.H. 2002: Offspring sex ratio and number in response to proportion of host sizes and ages in the parasitoid wasp Spalangia cameroni (Hymenoptera: Pteromalidae). - Environ. Entomol. 31: 505-508. Go to original source...
  24. Krainacker D.A., Carey J.R. & Vargas R.I. 1989: Size-specific survival and fecundity for laboratory strains of two tephritids (Diptera: Tephritidae) species: implications for mass rearing. - J. Econ. Entomol. 82: 104-108. Go to original source...
  25. Legner E.F. & Gerling D. 1967: Host-feeding and oviposition on Musca domestica by Spalangia cameroni, Nasonia vitripennis, and Muscidifurax raptor (Hymenoptera: Pteromalidae) influences their longevity and fecundity. - Ann. Entomol. Soc. Am. 60: 678-691. Go to original source...
  26. Liquido N.J., Shindoa L.A. & Cunningham R.T. 1991: Host Plants of the Mediterranean Fruit Fly, C. capitata (Wiedemann) (Diptera: Tephritidae): An Annotated World Review. Miscellaneous Publication 77. Entomological Society of America, Lanham, MD, 52 pp. Go to original source...
  27. Orozco D. & López R.O. 1993: Mating competitiveness of wild and laboratory mass-reared medflies: effect of male size. In Aluja M. & Liedo P. (eds): Fruit Flies: Biology and Management. Springer, New York, pp. 185-188. Go to original source...
  28. Papadopoulos N.T. 2008: Mediterranean fruit fly, Ceratitis capitata (Wiedemann) (Diptera: Tephritidae). In Capinera J.L. (ed.): Encyclopaedia of Entomology. Vol. 3. Springer, Heidelberg, pp. 2318-2322. 
  29. Pérez-Hinarejos M. & Beitia F. 2008: Parasitism of Spalangia cameroni (Hymenoptera, Pteromalidae), an idiobiont parasitoid of Ceratitis capitata (Diptera, Tephritidae). - IOBC/WPRS Bull. 38: 130-133.
  30. Rodriguero M.S., Vilardi J.C., Vera M.T., Cayol J.P. & Rial E. 2002: Morphometric traits and sexual selection in medfly (Diptera: Tephritidae) under field cage conditions. - Fla Entomol. 85: 143-149. Go to original source...
  31. Tormos J., Beitia F., Boeckmann E.A. & Asís J.D. 2009: The preimaginal stages and development of Spalangia cameroni Perkins (Hymenoptera: Pteromalidae) on Ceratitis capitata (Wiedemann) (Diptera: Tephritidae). - Micron 40: 646-658. Go to original source...
  32. Tormos J., Beitia F., Alonso M., Asís J.D. & Gayubo S. 2010: Assessment of Ceratitis capitata (Diptera: Tephritidae) pupae killed by heat or cold as hosts for rearing Spalangia cameroni (Hymenoptera: Pteromalidae). - Ann. Appl. Biol. 16: 179-185. Go to original source...
  33. Tormos J., Asís J.D., Sabater-Muñoz B., Baños L., Gayubo S.F. & Beitia F. 2012: Superparasitism in laboratory rearing of Spalangia cameroni (Hymenoptera: Pteromalidae) a parasitoid of medfly (Diptera: Tephritidae). - Bull. Entomol. Res. 102: 51-61. Go to original source...
  34. Tormos J., Sabater-Muñoz B., Asís J.D. & Beitia F. 2014: Validation of a methodology for rearing Spalangia cameroni (Hymenoptera: Pteromalidae) on Ceratitis capitata (Diptera: Tephritidae). - Can. Entomol. 146: 676-683. Go to original source...
  35. Tormos J., Beitia F., Asís J.D. & de Pedro L. 2018a: Natal host and learning as factors in host preference by Spalangia cameroni Perkins (Hymenoptera: Pteromalidae). - Crop Prot. 110: 155-159. Go to original source...
  36. Tormos J., Beitia F., Asís J.D. & de Pedro L. 2018b: Intraguild interactions between two biological control agents in citrus fruit: implications for biological control of medfly. - Ann. Appl. Biol. 172: 321-331. Go to original source...
  37. Zucoloto F.S. 1987: Feeding habits of Ceratitis capitata: Can larvae recognize a nutritional effective diet? - J. Insect Physiol. 33: 349-353. Go to original source...

This is an open access article distributed under the terms of the Creative Commons Attribution 4.0 International License (CC BY 4.0), which permits use, distribution, and reproduction in any medium, provided the original publication is properly cited. No use, distribution or reproduction is permitted which does not comply with these terms.